CA LIF ORNIA D EPA RTM EN T OF FOOD & AGRICULTURE California Pest Rating Proposal for Heterodera sturhani Subbotin 2015 Sturhan cereal cyst nematode Current Pest Rating: none Proposed Pest Rating: A Kingdom: Animalia, Phylum: Nematoda, Class: Secernentea, Subclass: Diplogasteria, Order: Tylenchida, Superfamily: Tylenchoidea, Family: Heteroderidae, Subfamily: Heteroderinae Comment Period: 04/26/2021 through 06/10/2021 Initiating Event: A pest risk assessment of Heterodera sturhani is presented here, and a pest rating for California is proposed. History & Status: Background: Cereal cyst nematodes are important pests that limit production of small grain cereals. Extensive nematode feeding reduces root mass and saps plant nutrients and can result in greatly reduced crop yields. Cyst nematodes are biotrophic sedentary endoparasites that can establish prolonged parasitic interactions with their hosts. They are among the most challenging nematodes to control, because of the "cyst" stage, which is the body of a dead female nematode containing hundreds of eggs. Cysts with viable eggs can persist in dry soil for years, where they remain relatively resistant to chemical and biological stresses. Cysts are easily moved with soil. There are many closely related cereal cyst nematode (CCN) species, and they are found in most regions of the world where small grains are grown. CCNs were first recognized in the 1940s and in the following decades were described in Russia, Ukraine, Latvia and other former republics of the U.S.S.R. Using morphological and molecular characteristics, the genus Heterodera has been divided into nine groups (Subbotin et al., 2010; Handoo and Subbotin, 2018). The Avenae group is one of the largest and contains species that parasitize monocots only. Molecular markers based on the internal transcribed CA LIF ORNIA D EPA RTM EN T OF FOOD & AGRICULTURE spacer (ITS) region of the ribosomal RNA gene and the cytochrome oxidase I gene can be used to differentiate species in this complex. Currently there are ten published species in the H. avenae complex: H. arenaria, H. avenae, H. aucklandica, H. australis, H. filipjevi, H. mani, H. pratensis, H. riparia, H. sturhani, and H. ustinovi. Five species from this group are considered as nematode pests and are collectively known as cereal cyst nematodes (CCN) (Smiley et al., 2017). Four are of major economic importance in cereal growing areas: the European CCN H. avenae, the Filipjev CCN H. filipjevi, the Sturhan CCN H. sturhani and the Australian CCN H. australis. The other six species in the complex parasitize grass species but have less importance to agriculture (Subbotin et al., 2018). In 2003 and 2010, Subbotin et al. noted samples identified as H. avenae from China were a distinct group within the H. avenae complex. The isolates they studied were morphologically and genetically closer to H. pratensis or H. riparia than to H. avenae, suggesting they may be another species. Sturhan and Rumpenhorst in 1996 had shown that Chinese cereal cyst nematode populations had a different IEF protein profile from H. avenae but did not separate them further. In 2015, Subbotin published an analysis of CoxI gene sequences which was evidence of a Chinese H. ‘avenae’ as separate from other species of the H. avenae complex. He formally described isolates from China previously identified as H. ‘avenae’ (type C) as a new species, H. sturhani, and gave it the common name Sturhan cereal cyst nematode. Surveys have shown that this nematode is widely distributed in provinces, autonomous regions, and cities in China, including Hubei, Shanxi, Henan, Hebei, Beijing, Inner Mongolia, Qinghai, Anhui, Shandong, Shaanxi, Gansu, Jiangsu, Tianjin, Tibet, and Xinjiang (Cui et al., 2015; D. L. Peng et al., 2009). Ongoing research recognizes H. avenae as a species complex and a dozen distinct species have been separated out (Subbotin et al., 2018). Precise species identification is important for implementing effective management practices as selection of resistant or tolerant cereal cultivars requires knowledge of individual species distributions, as cultivars are not necessarily resistant or tolerant to both (Yan et al., 3023). Heterodera sturhani is closely related to H. pratensis, but H. sturhani parasitizes cereals including wheat, barley, wild and cultivated oat, whereas H. pratensis is presently known only as a parasite of grasses (Subbotin et al., 2010). Hosts: The major cereal hosts are wheat (Triticum aestivum), oats (Avena sativa), and barley (Hordeum vulgare) but it also parasitizes grasses: Festuca arundinacea, Datylis glomerata, Phalaris tuberosa and others (Subbotin, 2015; Smiley et al., 2017). Symptoms: The diagnostic symptoms of cyst nematodes are usually the presence of cysts on the roots, the proliferation of roots, and shallow root systems. When there are population of Heterodera in the soil, patches of stunted seedlings (three- to five-leaf stage) can appear first. Stunted seedlings will exhibit chlorotic or necrotic lower leaves, with healthy younger leaves, few or no tillers, rotting of lower culms and crowns, and light brown roots with branching (Smiley et al., 2008). Plants produce smaller heads with shriveled grain kernels (Smiley et al., 2017). Heterodera sturhani differs from H. avenae by having smaller average cyst sizes and a smaller average fenestral length (Subbotin, 2015). Transmission: Heterodera sturhani completes one generation per year. A low temperature chill factor seems not to be involved in hatching, and the rate of hatch can be increased by cereal root exudates CA LIF ORNIA D EPA RTM EN T OF FOOD & AGRICULTURE (but exudates are not required). Juveniles begin to emerge from cysts during the autumn (October) and continue through spring (April) even in areas with cold winter climates. It does not seem to have a diapause requirement and can hatch anytime when hosts are available. Mobile, second-stage juveniles leave the cysts in the spring and burrow into the host roots just behind the growing point. They rest parallel to the main axis with their heads in the endodermis. The juveniles induce the formation of unique syncytial feeding structures as their sole nutrient resources within the vascular cylinder of the roots. After growing and molting for approximately 3 weeks, mobile, vermiform males are released back into the soil. The sedentary female matures 6 to 9 weeks after invasion. Her body breaks through the root surface but remain attached to the root. Males mate with adult females on the root surface. Females can lay and release 50-100 eggs into the soil. Near the end of her life, the female holds her eggs inside her body. The egg-filled female dies, and her body wall hardens to form a tough, leathery-skinned cyst around her eggs. The cysts are released into the soil as roots die (Willmott, 1972). The main way this nematode spreads locally is as cysts in the soil. Thus, anything that moves soil is a potential pathway including agricultural equipment and containers, tools, vehicle tires, and workers clothing or boots. Adults, juveniles, eggs, and cysts can be found in association with infected or contaminated planting stock. Cysts can also move in the soil with water from rainfall or irrigation. Cysts can persist in dry soil for months to years, protecting the eggs, until there is adequate water for hatching (Smiley et al., 2017). Damage Potential: Cereal cyst nematodes are among the most important nematode pests that limit production of small grain cereals worldwide, and Heterodera spp. are major pests of wheat, barley, and oat. Yield losses in China were previously attributed only to H. avenae could be from H. avenae, H. filipjevi, H. australis or H. sturhani, as all are present. Yield losses in three provinces of China, caused by ‘H. avenae,’ were estimated at 1.2 Mt, based on an infestation of 22% of the production area and an overall yield reduction of 10% in those areas (Peng et al. 2009). Worldwide Distribution: China (Subbotin et al., 2015). Official Control: Heterodera spp. is on the USDA’s harmful organism list for Australia, Chile, Jordan, Madagascar, Namibia, Nauru, Oman, South Africa, Syrian Arab Republic, and United Arab Emirates (USDA PCIT, 2021). California Distribution: None. California Interceptions: None The risk Heterodera sturhani would pose to California is evaluated below. Consequences of Introduction: CA LIF ORNIA D EPA RTM EN T OF FOOD & AGRICULTURE 1) Climate/Host Interaction: Heterodera sturhani has been found in diverse climates around the world and it is likely to become established wherever suitable hosts can grow. Wheat is the predominant small grain crop in California, grown on over 500,000 acres, with small grains serving as important rotational crops (UC Agronomy Research and Information Center: Small Grains; Chitambar et al., 2018). Evaluate if the pest would have suitable hosts and climate to establish in California. Score: 3 - Low (1) Not likely to establish in California; or likely to establish in very limited areas. - Medium (2) may be able to establish in a larger but limited part of California. - High (3) likely to establish a widespread distribution in California. 2) Known Pest Host Range: The host range contains cereals and grasses in the family Poaceae. Evaluate the host range of the pest. Score: 2 - Low (1) has a very limited host range. - Medium (2) has a moderate host range. - High (3) has a wide host range. 3) Pest Reproductive Potential: Tens to hundreds of eggs can be produced while the female is alive, with an additional ten to hundreds retained within her cyst after her death. For long and short distance dispersal these nematodes are dependent on movements of cysts, cyst-infested soils, and cyst-infested seed lots. Evaluate the natural and artificial dispersal potential of the pest. Score: 2 - Low (1) does not have high reproductive or dispersal potential. - Medium (2) has either high reproductive or dispersal potential. - High (3) has both high reproduction and dispersal potential.